Opinion
Theoretical motivations for investigating the neural correlates of consciousness Hakwan Lau∗
I review the major contenders for the neural correlates of visual awareness. Different views of the neural correlates turn out to support different theories, such as the global workspace theory, local visual processing theories, and the higher-order representation theory. Therefore, studying the neural correlates of consciousness may prove useful to theoretical development, although arbitrating between different interpretations of the neural results may involve conceptual issues as well. 2010 John Wiley & Sons, Ltd. WIREs Cogn Sci 2011 2 1–7 DOI: 10.1002/wcs.93
INTRODUCTION
I
nvestigations of the neural correlates of consciousness (NCC1 ) have gained popularity over recent years. Researchers typically look for a difference in neural activity that reflects a difference in conscious perception; a good portion of such a research has been carried out in the visual modality. As we gather more and more results, perhaps it is a good time to reflect on why we want to study the NCC in the first place. What is the advantage of finding the NCC? What would they tell us? Consciousness is no doubt one of the most intriguing problems in science.1,2 To some, it is a test of the limits of cognitive science, as it is not yet clear what a cognitive explanation of phenomenal consciousness might even look like. How might identifying the NCC shed light on these perplexing issues? A particular area of concern is that many current studies on the NCC employ methods such as fMRI. Typically, the results give rough maps of activation patterns over the whole brain. What could we possibly learn if the NCC at this level of analysis turns out to be one pattern of activations rather than another? Is it not just neo-phrenology? This article outlines some reflections on these issues. I first review the current major contenders for the visual NCC (at the level of whole-brain functional anatomy). I then argue that different cognitive/philosophical theories of consciousness would ∗ Correspondence
to: [email protected]
Department of Psychology, Columbia University, New York, NY, USA DOI: 10.1002/wcs.93
Vo lu me 2, Jan u ary /Febru ary 2011
in fact be supported by different results. Therefore, identifying the NCC is informative to theoretical developments.
VIEWS OF NCC ‘Dominant’ View of NCC: Frontoparietal Network Plus Extrastriate Correlates One popular view of the visual NCC,3,4 at least up to about 5 years ago, is as follows:(1) the primary visual cortex (V1) is perhaps necessary for visual awareness but the representations are too fine-grained to reflect the conscious content; (2) the specific conscious content is represented in the relevant extrastriate areas, such as the fusiform face area (FFA) for the conscious percept of a face; and (3) activity in the prefrontal and parietal cortices is another enabling factor, which is essential for visual awareness to occur. In other words, the NCC is rather widespread throughout the cortex. This view is perhaps not exactly the consensus, but it certainly is one of the most popular and is well supported by numerous highprofile imaging studies.3,4 For instance, contrasting conscious perception of visible words against presentation of invisible masked words found more activity in the content-specific extrastriate area that is associated with word perception.5 Additionally, there was widespread activity in the prefrontal and parietal cortices, found only with conscious perception but not with presentation of invisible masked words.
Alternative 1: Visual Activity Only An alternative view of the visual NCC has recently been gaining popularity.6–9 According to this view,
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the activity in the prefrontal and parietal areas is not essential. Rather, they reflect attention and access to the specific content, or the reporting mechanism. That is, when subjects are consciously seeing a certain stimulus (as compared to not consciously seeing it), they may pay more attention to it, or try to think more about it, remember it, or otherwise give more cognitive access to the information regarding the visual stimulus. Also, the subjects usually have to report what they see to the experimenter. According to this alternative view, the activity in the prefrontal and parietal cortices reflects these associated processes, but not conscious perception per se. There is one study10 where researchers controlled for the subject’s attention by directing the focus of attention away from the stimulus in question. Subjects performed a difficult detection task at fixation, while the rest of the visual field contained a pattern that was either flickering or static because the flicker had been ‘masked out’. The visible flicker (as compared to masked flicker) induced activity in the visual cortex, but not in the prefrontal or parietal areas. The argument is that subjects put most of their attentional resources at the fixation task, and therefore the visibility of the flicker did not affect activity in the prefrontal and parietal areas. This seems to suggest that visibility itself is not necessarily linked to activity in the prefrontal and parietal areas. When Macknik, one of the researchers in that study,10 presented the results at the eighth conference of the Association for the Scientific Study of Consciousness in Antwerp, Belgium, I recall that it was met with considerable skepticism. However, a similar study has subsequently been performed, which generally confirmed the results. In that newer study11 visible words were used as stimuli. Again, it was found that when subjects did not have to report about the stimuli in question, there was no activity in the prefrontal or parietal areas that reflected the visibility of the words. In another study,12 it was found that when the visual stimulus presentation rate increased, activity in the prefrontal cortex would decrease. Subjects performed a categorization task on pictures. Comparing the condition where the pictures were presented at a high rate against the condition where the rate was low, there was increased activity in the visual areas, but a decrease in activity in prefrontal areas that is related to self-introspection. However, note that this prefrontal area (superior frontal gyrus) is not an area that is usually associated with visual awareness in a positive way (usually it is the dorsolateral prefrontal cortex, DLPFC, and the frontal eye fields). Moreover, it could be argued that when pictures were 2
presented at a high rate, subjects were no longer seeing each individual picture as clearly. In fact, subjects’ performance decreased when the pictures were presented at a higher rate. Therefore it is unclear whether the condition with the higher presentation rate indeed induced higher levels of visual awareness. The view that prefrontal activity is not essential to visual awareness per se is compatible with the claim that lesions to prefrontal regions do not seem to abolish visual awareness.13 This has often been taken to argue that activity in the prefrontal cortex may be more of an epiphenomenon than the essential enabling factor. However, some recent studies have shown that lesion to prefrontal cortex can in fact influence visual awareness. In particular, after prefrontal lesion, the subjective reports of awareness seem to be more affected than the forced-choice task performance.14 Subjective reports of awareness refer to ratings or answers given in response to questions such as ‘Did you see the identity of the target or did you just guessed?’, or ‘Are you very sure of your response or not?’. We have conducted another study employing transcranial magnetic stimulation (TMS).15 We found that subjective report of awareness, but not forcedchoice task performance, was affected after TMS was applied to the prefrontal cortex. The distinction between subjective reports and forced-choice task performance is critical for the view discussed in the next section.
Alternative 2: Prefrontal and/or Parietal Activity Only Another alternative view of the NCC is that most of what has been claimed to be the NCC is in fact reflecting signal strength or performance capacity, but not conscious awareness per se.16 In most studies of the NCC, researchers try to show that in one condition subjects could see the visual stimuli, and in another condition they could not. While there is clearly a difference in level of visual awareness, there are other potential confounds too. When subjects are seeing the stimuli clearly, they are more capable of performing tasks in relation to the stimuli. When subjects could not see the stimuli (e.g., because the stimuli has been rendered invisible by masking), they are usually unable to perform tasks to identify the stimuli. Even when no such task is required of the subjects, one could still argue that the difference is really that in the ‘conscious’ condition there is a strong signal in the brain, and in the ‘unconscious’ condition the signal is weak or absent. Is visual awareness just the same as having a strong enough signal? One could argue that this is not true. Signal strength or task performance capacity may be
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a relatively objective aspect of visual perception that does not reflect the subjective nature of visual awareness. In patients with blind sight, task performance for visual discrimination could be well above chance, and yet visual awareness is reported to be completely absent. Lau and Passingham17 have demonstrated such dissociation between performance capacity and subjectively reported level of awareness in healthy volunteers. Using a paradigm based on metacontrast masking, they were able to create task conditions where the performance for discriminating two targets was matched, and yet subjects reported different frequencies of seeing the targets consciously. When they compared the associated neural activity for the two conditions in the fMRI scanner, they found a difference in activity in the DLPFC. Incidentally, there was also a previous report on a blindsight patient which argues that the DLPFC is important for visual awareness.18 One notable finding is that Lau and Passingham17 were unable to find a difference in the visual areas. This is quite striking given that this was a visual manipulation in a visual task, which led to a difference in visual awareness. Their interpretation is that such a difference was not found in the visual areas because the performance capacity was matched; the visual areas reflect visual signal, which drives performance. But it is not the same as the subjective conscious experience. The authors, together with other colleagues, have subsequently gone on to apply TMS to this area in the prefrontal cortex.15 And as expected, TMS did not affect the task performance. However, it changed the way subjects placed the subjective ratings of visibility.a The details of this alternative proposal are not yet clear. It is hard to imagine that activity in the DLPFC alone is sufficient to determine the subjective aspects of visual awareness. However, the key point is that we should distinguish between the signal strength, or the task performance capacity, and the reports of subjective experience. If we control for signal strength, the subjective reports of conscious experience may well be reflected by activity in the association cortices alone (e.g., prefrontal and parietal areas).
THEORIES OF CONSCIOUSNESS AND HOW THEY ARE SUPPORTED BY DIFFERENT VIEWS OF NCCs Global Theories Many have taken the first view (i.e., the ‘dominant’ view) of the NCC as support for a certain class of Vo lu me 2, Jan u ary /Febru ary 2011
theories. For instance, the global workspace theory proposed by Baars19 (reviewed in 2005), and later embellished in neuronal terms by Dehaene and colleagues,4 would predict results similar to what I have called the dominant view. According to the global workspace theory, there exists a central broadcasting mechanism that allows the flexible and global exchange of information between peripheral modules (such as early vision, low level motor processing, and memory). When information enters this workspace, it becomes conscious, and is globally broadcasted to all modules and therefore all subsystems can share and edit such information. Dehaene and colleagues specifically hypothesize that the workspace depends on neurons in the prefrontal and parietal areas.b Tononi’s information integration theory20 is supposed to be substrate independent. However, according to that theory, consciousness depends on a subset of neurons in the brain that forms complex connections, and thereby the dynamic ‘core’ that supports conscious experiences. The connections in the cerebellum, for instance, are dense, but the pattern is not complex enough according to the formal measures of the theory to count as part of the ‘core’. It is sometimes speculated that the thalamic–cortical system is part of this ‘core’. One may think that with their dense and varied connections, the prefrontal and parietal cortices may also be suitable candidates to be part of this ‘core’ that supports conscious experience. Therefore, to a certain extent the information integration theory is supported by this first view of the NCC too.
Local Theories If it turns out to be true that the visual NCC consists of only activity in the posterior visual areas in the brain, theories other than the global workspace would be supported. Block,7,8 for instance, put forward what he sometimes calls the ‘biological’ theory, which says that phenomenal visual awareness depends on specific biological substrates in the posterior visual areas in the brain. Prefrontal areas support cognitive access to such a posterior system, and the former has a smaller informational capacity than the latter; the two are therefore distinct.c Lamme9 similarly argues that visual awareness depends on local feedback loops within the visual areas. Processing in higher areas is related to attention, which is distinct from awareness itself.21 Similarly, Zeki22 has proposed what is called the ‘micro-consciousness’ theory, which suggests that activity in the early visual areas are the correlates of specific conscious percepts.
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Many of these theories are controversial, and some pose conflicts to each other. However, one common theme here is that the neural substrate that supports the processing of visual information itself is sufficient to generate a conscious percept, without the need for further processing in higher cognitive areas. In philosophy, one relevant and perhaps similar theory is representationalism,23,24 which (roughly) holds that the phenomenal character associated with a perceptual event is determined by the content of the relevant representation. Mostly, the relevant representation here refers to the ‘first-order’ representation, i.e., if you are seeing a house, the phenomenal character is determined by the content of the representation that is about the house. There is another kind of representationalism that involves what are called ‘higher-order’ representations, to which we now turn.
Higher-Order Theories According to higher-order representational theories,25–27 in order to have a conscious experience, we need more than just the first-order representation, which has the object of perception as its content. On top of that, we need to have a higher-order representation that is about the first-order representation. There is some debate as to whether the content of this higher-order representation is similar to thoughts25 or percepts,26 or perhaps that the higher-order representation and the first-order representation should not be counted as separate, but rather as parts of a single self-referential system.27 According to the higher-order thought theory, which is arguably the most popular view amongst the different versions, the content of the higher-order representation is something like ‘I think I’m seeing red’, given that the first-order representation is ‘red’. I have put forward a different version of this theory.16 According to this theory, the higher-order representation simply enables statistical inferences or judgments of perceptual certainty. That is, given that the first-order representations are often corrupted by noise in the brain, the higher-order representation contains some statistical information that allows one to say something like ‘this perception (of a house) is likely to be 99% reliable’. Awareness occurs when a percept is correctly judged to be sufficiently reliable. There are, I think, some advantages of this version of higherorder representationalism over the traditional philosophical forms,16 but these are not discussed here. Higher-order theories in general are congenial to the results that a change in activity in the prefrontal and parietal cortices are sufficient for a change in conscious percept (Alternative 2)—one would expect the higher-order representations to be in these brain 4
regions, as they seem to play roles in uncertainty monitoring, cognitive control, thinking and planning, etc. In particular, some higher-order theorists (myself included) are committed to make the prediction that if one keeps the first-order representation constant, a change in the higher-order representations alone would be enough to change the character of a conscious experience.d This last point is important and is perhaps what distinguishes at least some higher-order theories from the global workspace theory. It is unclear whether the global workspace theory is committed to such predictions. In most discussions, one typically thinks that a visual signal (roughly equivalent to a first-order representation) enters the global workspace by being stronger than other competing signals. Therefore, when a visual percept changes from consciously seen to unseen, one would expect the difference to be reflected not only in the higher global workspace areas, but in the lower visual signals too. Also, it may be possible that when the signal enters the workspace, the global broadcasting sends feedback to the earlier visual areas, which would in turn mean that the conscious signal would end up becoming stronger in the early areas. Even when the first-order visual signal is the same, and somehow in one condition the signal gets into the workspace and in another condition it does not, one would predict big behavioral differences, such as that in one condition the visual targets are better identified or reported, because the workspace is supposed to be functionally important. The higher-order theory (at least the version I put forward), however, would expect that there can be few functional differences in terms of discrimination, identification, or ability to report the target, if the first-order signal/representation is kept the same. A difference in higher-order representation leads to a difference in awareness, and the only accompanying behavioral difference is the judgment of perceptual certainty. For example, the subject reports ‘red’ in both cases with equal accuracy across many trials, except that with the right higher-order representation the subject would say ‘I’m consciously seeing red and I’m confident that I’m right’; while with the faulty higher-order representation the subject would say ‘I don’t consciously see anything but if you force me to guess, my hunch is there’s something red’.
DUAL CHANNEL VERSUS HIERARCHICAL PROCESSING The last point is critically relevant to what the difference is between normal vision and blindsight.
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One advantage of higher-order theory is that it explains blindsight behavior most naturally. In blindsight, the performance capacity is above chance, presumably because some residual visual signal (firstorder representations) still exists. What are missing are the relevant higher-order representations (perhaps because the cortical signal is disturbed due to the damage in V1), which leads to a dramatically reduced level of perceptual certainty. In fact, one can have perfectly matched performance capacity between blindsight and normal vision (by for instance presenting a strong stimulus to blindsighted vision and a weak stimulus to normal vision), and the prediction would be that the difference in awareness would be reflected in the prefrontal and parietal areas. Indeed, there is some evidence supporting this.18,28 How would the global workspace theory account for this kind of performance-matched condition where the subjectively reported levels of awareness differ dramatically? If the visual signal (first-order representation) itself is the same, and that gets into the workspace in one condition but not the other, one would expect a difference in performance capacity because the workspace is supposed to contribute to that. One could perhaps maintain that some signal can get into the workspace, and thereby render itself conscious, without influencing task performance. However, the main point of the workspace is to amplify and broadcast the signal, for functional reasons. If one allows signal to enter the workspace without having any functional consequence but just to make itself conscious, it would no longer be in the spirit of the workspace theory. Recently, one of the major proponents of the global workspace theory, Stanislas Dehaene, together with colleagues, has proposed a dual-channel model that would account for unconscious but functionally strong behavior.14 Essentially, the idea is that sometimes the signal can enter some other channel rather than the global workspace, which can also contribute to performance capacity. Allowing for such a ‘backdoor’ of information processing somewhat makes the global workspace not so ‘global’, but this accounts for phenomena such as blindsight. It should be easy to see that this dual-channel structure is a natural solution for the local theorist too. According to them, the early visual signal itself (the first-order representation) is sufficient for visual awareness. So how can one explain blindsight then? How can you have a visual signal without awareness? Presumably, some other visual signal, perhaps carried by a different kind of neural substrate that does not lead to awareness, would do the unconscious job. Vo lu me 2, Jan u ary /Febru ary 2011
This again means that there are different channels of processing, some conscious and some not. Local theorists may try to argue that the same sensory signal is partially impaired in blindsight, which leads to unawareness. For instance, it could be that feedback processing to V1 is no longer possible, which leads to unawareness. However, if feedback to V1 is part of the signal, when this breaks down one would expect performance to go down as well. The focus here is on how to explain performance-matched cases of difference in awareness. In such cases, it would be natural for local theorists to assume that some other ‘unconscious’ signal arises to compensate for the loss of the ‘conscious’ signal. This is the critical point where the higher-order theories differ from both the global and local theories. According to higher-order theories, one could have exactly the same channel, but some late stage of processing up in the hierarchy (the higher-order representation stage) differs, and this is all that is sufficient to render a conscious percept unconscious. In fact, there are some preliminary results from my laboratory, using computational modeling, which suggest that a hierarchical model of processing is more realistic than a dual-channel model in terms of accounting for the differences between conscious and unconscious vision.29 In neural terms, this means that the burden falls on global and local theorists to identify neural substrates in presumably different neuronal populations that subserve unconscious visual behavior, as their theories seem to require a different channel for unconscious processing. The higher-order theorists (or at least some of them) are not committed to this. A subject could have exactly the same visual processing in visual and subcortical areas, and so long as some activity in higher-order monitoring areas differs, one could render normal vision unconscious.
CONCLUDING REMARKS I do not pretend that this is an unbiased review. It should come as no surprise that the author prefers the higher-order theory, and I think that one could keep the visual activity constant and yet manipulate visual phenomenology by changing the activity in prefrontal and parietal areas. On some occasions, to support such opinions I even appeal to preliminary data (i.e., conference posters and abstracts, but not full published papers). But opinions aside, the main point of the article is not to convince you that one theory is right over the others. The point is that by studying the NCC, one could, in fact, make theoretical contributions.
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However, as we look into this issue in more detail, it may become obvious that the problem does not afford such a clean-cut solution. It is not as if the problem of deciding different views of the NCC can be resolved solely by experimental labor. The issue often involves deciding what counts as an experimental confound and what counts as a good experiment. Should we distinguish between attention and awareness, or treat them as the same? Is awareness the same as performance capacity? When we keep the stimulus constant, and compare ‘hits’ versus ‘misses’, are we looking at awareness, or just spontaneous fluctuations of the signal strength? I have given arguments elsewhere30 to support my view that comparing ‘hits’ versus ‘misses’ is perhaps flawed (it studies performance capacity but not awareness per se), and that perceptual certainty is probably what tracks the subjective aspects of awareness best. But these arguments are controversial, and I do not wish to repeat them here. It may be unfortunate that we cannot just quickly and unanimously derive some empirical predictions based on the theories, and arbitrate them by some uncontroversial experiments on the NCC. The search for the NCC is bound to involve conceptual problems. But if anything, I hope I have convinced some readers that the search for the NCC is not completely irrelevant to our theoretical understanding of the nature of perceptual awareness. The future depends much on the interplay between both theory and empirical studies.
NOTES a
The result was independently predicted by philosopher Uriah Kriegel.31
b
For most of the discussion on the relationship between theories and views of NCCs, one could think of the theory as predicting a certain NCC to be the necessary condition for consciousness to arise. In this case of the global workspace theory, though, it is not entirely clear whether all global theorists hold that early visual activity is necessary. That is, such an activity could be the normal cause that leads to global activity in the prefrontal and parietal cortex, which in turn is necessary for consciousness. c Technically, Block’s theory is about the experiential/phenomenological aspect of consciousness whereas the global workspace theory concerns conscious access of information. So in one sense, the two theories do not contradict. However, many who reject Block’s theory also reject his distinction of phenomenology versus access; many would say phenomenology that is not accessible should not be considered conscious at all. Therefore, Block’s theory and the global workspace theory are often seen as in competition. d Theorists like myself and Uriah Kriegel predict this to be the case because we think the overall phenomenology, i.e., content of awareness, is determined jointly by the first-order and higher-order representations. In my view specifically, I think the higher-order representations do not duplicate the perceptual content of the first-order representations. Rather, metaphorically speaking, they add a ‘label’ to the first-order representations to explicitly indicate how reliable they are. Higher-order thought theorist David Rosenthal, on the other hand, holds that the content of the higherorder representation alone is sufficient to determine the content of awareness.
REFERENCES 1. Crick F, Koch C. A framework for consciousness. Nat Neurosci 2003, 6:119–126.
word masking and unconscious repetition priming. Nat Neurosci 2001, 4:752–758.
2. Chalmers DJ. The puzzle of conscious experience. Sci Am 1995, 273:80–86.
6. Macknik SL. Visual masking approaches to visual awareness. Prog Brain Res 2006, 155:177–215.
3. Rees G, Kreiman G, Koch C. Neural correlates of consciousness in humans. Nat Rev Neurosci 2002, 3:261–270.
7. Block N. Two neural correlates of consciousness. Trends Cogn Sci 2005, 9:46–52.
4. Sergent C, Dehaene S. Neural processes underlying conscious perception: experimental findings and a global neuronal workspace framework. J Physiol Paris 2004, 98:374–384. 5. Dehaene S, Naccache L, Cohen L, Bihan DL, Mangin JF, Poline JB, Rivi`ere D. Cerebral mechanisms of
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8. Block N. Consciousness, accessibility, and the mesh between psychology and neuroscience. Behav Brain Sci 2007, 30:481–499. 9. Lamme VA. Towards a true neural stance on consciousness. Trends Cogn Sci 2006, 10:494–501. 10. Tse PU, Martinez-Conde S, Schlegel AA, Macknik SL. Visibility, visual awareness, and visual masking
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of simple unattended targets are confined to areas in the occipital cortex beyond human V1/V2. Proc Natl Acad Sci U S A 2005, 102:17178–17183. 11. Kouider S, Dehaene S, Jobert A, Le Bihan D. Cerebral bases of subliminal and supraliminal priming during reading. Cereb Cortex 2007, 17:2019–2029. 12. Goldberg II, Harel M, Malach R. When the brain loses its self: prefrontal inactivation during sensorimotor processing. Neuron 2006, 50:329–339. 13. Pollen DA. Cortical areas in visual awareness. Nature 1995, 377:293–295. 14. Del Cul A, Dehaene S, Reyes P, Bravo E, Slachevsky A. Causal role of prefrontal cortex in the threshold for access to consciousness. Brain 2009, 132:2531–2540. 15. Maniscalco B, Rounis E, Rothwell J, Passingham RE, Lau H. Theta-burst transcranial magnetic stimulation to the prefrontal cortex impairs metacognitive visual awareness Vision Sciences Society meeting abstract as published in Journal of Vision, 2009. 16. Lau HC. A higher order Bayesian decision theory of consciousness. Prog Brain Res 2008, 168:35–48. 17. Lau HC, Passingham RE. Relative blindsight in normal observers and the neural correlate of visual consciousness. Proc Natl Acad Sci U S A 2006, 103:18763–18768.
20. Tononi G. An information integration theory of consciousness. BMC Neurosci 2004, 5:42. 21. Koch C, Tsuchiya N. Attention and consciousness: two distinct brain processes. Trends Cogn Sci 2007, 11:16–22. 22. Zeki S. The disunity of consciousness. Prog Brain Res 2008, 168:11–18. 23. Dretske F. Naturalizing the Mind. Cambridge, MA: MIT Press; 1995. 24. Tye M. Ten Problems of Consciousness. Cambridge, MA: MIT Press; 1995. 25. Rosenthal D. Consciousness and Mind. New York, NY: Oxford University Press; 2005. 26. Lycan W. Consciousness and Experience. Cambridge, MA: Bradford Books/MIT Press; 1996. 27. Kriegel U. Subjective Consciousness: A SelfRepresentational Theory. Oxford, UK: Oxford University Press; 2009. 28. Persaud N, Davidson M, Mobbs D, Cowey A, Passingham RE, Lau H. Awareness-related activity in prefrontal and parietal cortices reflects more than superior visual performance capacity: A blindsight case study (manuscript in preparation). 29. Maniscalco B. Lau H. Evaluating signal detection models of perceptual decision confidence, Abstract for Computational and System Neuroscience meeting 2009.
18. Sahraie A, Weiskrantz L, Barbur JL, Simmons A, Williams SC, Brammer MJ. Pattern of neuronal activity associated with conscious and unconscious processing of visual signals. Proc Natl Acad Sci U S A 1997, 94:9406–9411.
30. Lau H. Are we studying consciousness yet? In: Weiskrantz L, Davies M, eds. Frontiers of Consciousness: Chichele Lectures. Oxford, UK: Oxford University Press; 2008a.
19. Baars BJ. Global workspace theory of consciousness: toward a cognitive neuroscience of human experience. Prog Brain Res 2005, 150:45–53.
31. Kriegel U. A cross-order integration hypothesis for the neural correlate of consciousness. Consciousness and Cognition 2007, 16:897–912.
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Theoretical motivations for investigating the neural correlates of consciousness Hakwan Lau∗
I review the major contenders for the neural correlates of visual awareness. Different views of the neural correlates turn out to support different theories, such as the global workspace theory, local visual processing theories, and the higher-order representation theory. Therefore, studying the neural correlates of consciousness may prove useful to theoretical development, although arbitrating between different interpretations of the neural results may involve conceptual issues as well. 2010 John Wiley & Sons, Ltd. WIREs Cogn Sci 2011 2 1–7 DOI: 10.1002/wcs.93
INTRODUCTION
I
nvestigations of the neural correlates of consciousness (NCC1 ) have gained popularity over recent years. Researchers typically look for a difference in neural activity that reflects a difference in conscious perception; a good portion of such a research has been carried out in the visual modality. As we gather more and more results, perhaps it is a good time to reflect on why we want to study the NCC in the first place. What is the advantage of finding the NCC? What would they tell us? Consciousness is no doubt one of the most intriguing problems in science.1,2 To some, it is a test of the limits of cognitive science, as it is not yet clear what a cognitive explanation of phenomenal consciousness might even look like. How might identifying the NCC shed light on these perplexing issues? A particular area of concern is that many current studies on the NCC employ methods such as fMRI. Typically, the results give rough maps of activation patterns over the whole brain. What could we possibly learn if the NCC at this level of analysis turns out to be one pattern of activations rather than another? Is it not just neo-phrenology? This article outlines some reflections on these issues. I first review the current major contenders for the visual NCC (at the level of whole-brain functional anatomy). I then argue that different cognitive/philosophical theories of consciousness would ∗ Correspondence
to: [email protected]
Department of Psychology, Columbia University, New York, NY, USA DOI: 10.1002/wcs.93
Vo lu me 2, Jan u ary /Febru ary 2011
in fact be supported by different results. Therefore, identifying the NCC is informative to theoretical developments.
VIEWS OF NCC ‘Dominant’ View of NCC: Frontoparietal Network Plus Extrastriate Correlates One popular view of the visual NCC,3,4 at least up to about 5 years ago, is as follows:(1) the primary visual cortex (V1) is perhaps necessary for visual awareness but the representations are too fine-grained to reflect the conscious content; (2) the specific conscious content is represented in the relevant extrastriate areas, such as the fusiform face area (FFA) for the conscious percept of a face; and (3) activity in the prefrontal and parietal cortices is another enabling factor, which is essential for visual awareness to occur. In other words, the NCC is rather widespread throughout the cortex. This view is perhaps not exactly the consensus, but it certainly is one of the most popular and is well supported by numerous highprofile imaging studies.3,4 For instance, contrasting conscious perception of visible words against presentation of invisible masked words found more activity in the content-specific extrastriate area that is associated with word perception.5 Additionally, there was widespread activity in the prefrontal and parietal cortices, found only with conscious perception but not with presentation of invisible masked words.
Alternative 1: Visual Activity Only An alternative view of the visual NCC has recently been gaining popularity.6–9 According to this view,
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the activity in the prefrontal and parietal areas is not essential. Rather, they reflect attention and access to the specific content, or the reporting mechanism. That is, when subjects are consciously seeing a certain stimulus (as compared to not consciously seeing it), they may pay more attention to it, or try to think more about it, remember it, or otherwise give more cognitive access to the information regarding the visual stimulus. Also, the subjects usually have to report what they see to the experimenter. According to this alternative view, the activity in the prefrontal and parietal cortices reflects these associated processes, but not conscious perception per se. There is one study10 where researchers controlled for the subject’s attention by directing the focus of attention away from the stimulus in question. Subjects performed a difficult detection task at fixation, while the rest of the visual field contained a pattern that was either flickering or static because the flicker had been ‘masked out’. The visible flicker (as compared to masked flicker) induced activity in the visual cortex, but not in the prefrontal or parietal areas. The argument is that subjects put most of their attentional resources at the fixation task, and therefore the visibility of the flicker did not affect activity in the prefrontal and parietal areas. This seems to suggest that visibility itself is not necessarily linked to activity in the prefrontal and parietal areas. When Macknik, one of the researchers in that study,10 presented the results at the eighth conference of the Association for the Scientific Study of Consciousness in Antwerp, Belgium, I recall that it was met with considerable skepticism. However, a similar study has subsequently been performed, which generally confirmed the results. In that newer study11 visible words were used as stimuli. Again, it was found that when subjects did not have to report about the stimuli in question, there was no activity in the prefrontal or parietal areas that reflected the visibility of the words. In another study,12 it was found that when the visual stimulus presentation rate increased, activity in the prefrontal cortex would decrease. Subjects performed a categorization task on pictures. Comparing the condition where the pictures were presented at a high rate against the condition where the rate was low, there was increased activity in the visual areas, but a decrease in activity in prefrontal areas that is related to self-introspection. However, note that this prefrontal area (superior frontal gyrus) is not an area that is usually associated with visual awareness in a positive way (usually it is the dorsolateral prefrontal cortex, DLPFC, and the frontal eye fields). Moreover, it could be argued that when pictures were 2
presented at a high rate, subjects were no longer seeing each individual picture as clearly. In fact, subjects’ performance decreased when the pictures were presented at a higher rate. Therefore it is unclear whether the condition with the higher presentation rate indeed induced higher levels of visual awareness. The view that prefrontal activity is not essential to visual awareness per se is compatible with the claim that lesions to prefrontal regions do not seem to abolish visual awareness.13 This has often been taken to argue that activity in the prefrontal cortex may be more of an epiphenomenon than the essential enabling factor. However, some recent studies have shown that lesion to prefrontal cortex can in fact influence visual awareness. In particular, after prefrontal lesion, the subjective reports of awareness seem to be more affected than the forced-choice task performance.14 Subjective reports of awareness refer to ratings or answers given in response to questions such as ‘Did you see the identity of the target or did you just guessed?’, or ‘Are you very sure of your response or not?’. We have conducted another study employing transcranial magnetic stimulation (TMS).15 We found that subjective report of awareness, but not forcedchoice task performance, was affected after TMS was applied to the prefrontal cortex. The distinction between subjective reports and forced-choice task performance is critical for the view discussed in the next section.
Alternative 2: Prefrontal and/or Parietal Activity Only Another alternative view of the NCC is that most of what has been claimed to be the NCC is in fact reflecting signal strength or performance capacity, but not conscious awareness per se.16 In most studies of the NCC, researchers try to show that in one condition subjects could see the visual stimuli, and in another condition they could not. While there is clearly a difference in level of visual awareness, there are other potential confounds too. When subjects are seeing the stimuli clearly, they are more capable of performing tasks in relation to the stimuli. When subjects could not see the stimuli (e.g., because the stimuli has been rendered invisible by masking), they are usually unable to perform tasks to identify the stimuli. Even when no such task is required of the subjects, one could still argue that the difference is really that in the ‘conscious’ condition there is a strong signal in the brain, and in the ‘unconscious’ condition the signal is weak or absent. Is visual awareness just the same as having a strong enough signal? One could argue that this is not true. Signal strength or task performance capacity may be
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a relatively objective aspect of visual perception that does not reflect the subjective nature of visual awareness. In patients with blind sight, task performance for visual discrimination could be well above chance, and yet visual awareness is reported to be completely absent. Lau and Passingham17 have demonstrated such dissociation between performance capacity and subjectively reported level of awareness in healthy volunteers. Using a paradigm based on metacontrast masking, they were able to create task conditions where the performance for discriminating two targets was matched, and yet subjects reported different frequencies of seeing the targets consciously. When they compared the associated neural activity for the two conditions in the fMRI scanner, they found a difference in activity in the DLPFC. Incidentally, there was also a previous report on a blindsight patient which argues that the DLPFC is important for visual awareness.18 One notable finding is that Lau and Passingham17 were unable to find a difference in the visual areas. This is quite striking given that this was a visual manipulation in a visual task, which led to a difference in visual awareness. Their interpretation is that such a difference was not found in the visual areas because the performance capacity was matched; the visual areas reflect visual signal, which drives performance. But it is not the same as the subjective conscious experience. The authors, together with other colleagues, have subsequently gone on to apply TMS to this area in the prefrontal cortex.15 And as expected, TMS did not affect the task performance. However, it changed the way subjects placed the subjective ratings of visibility.a The details of this alternative proposal are not yet clear. It is hard to imagine that activity in the DLPFC alone is sufficient to determine the subjective aspects of visual awareness. However, the key point is that we should distinguish between the signal strength, or the task performance capacity, and the reports of subjective experience. If we control for signal strength, the subjective reports of conscious experience may well be reflected by activity in the association cortices alone (e.g., prefrontal and parietal areas).
THEORIES OF CONSCIOUSNESS AND HOW THEY ARE SUPPORTED BY DIFFERENT VIEWS OF NCCs Global Theories Many have taken the first view (i.e., the ‘dominant’ view) of the NCC as support for a certain class of Vo lu me 2, Jan u ary /Febru ary 2011
theories. For instance, the global workspace theory proposed by Baars19 (reviewed in 2005), and later embellished in neuronal terms by Dehaene and colleagues,4 would predict results similar to what I have called the dominant view. According to the global workspace theory, there exists a central broadcasting mechanism that allows the flexible and global exchange of information between peripheral modules (such as early vision, low level motor processing, and memory). When information enters this workspace, it becomes conscious, and is globally broadcasted to all modules and therefore all subsystems can share and edit such information. Dehaene and colleagues specifically hypothesize that the workspace depends on neurons in the prefrontal and parietal areas.b Tononi’s information integration theory20 is supposed to be substrate independent. However, according to that theory, consciousness depends on a subset of neurons in the brain that forms complex connections, and thereby the dynamic ‘core’ that supports conscious experiences. The connections in the cerebellum, for instance, are dense, but the pattern is not complex enough according to the formal measures of the theory to count as part of the ‘core’. It is sometimes speculated that the thalamic–cortical system is part of this ‘core’. One may think that with their dense and varied connections, the prefrontal and parietal cortices may also be suitable candidates to be part of this ‘core’ that supports conscious experience. Therefore, to a certain extent the information integration theory is supported by this first view of the NCC too.
Local Theories If it turns out to be true that the visual NCC consists of only activity in the posterior visual areas in the brain, theories other than the global workspace would be supported. Block,7,8 for instance, put forward what he sometimes calls the ‘biological’ theory, which says that phenomenal visual awareness depends on specific biological substrates in the posterior visual areas in the brain. Prefrontal areas support cognitive access to such a posterior system, and the former has a smaller informational capacity than the latter; the two are therefore distinct.c Lamme9 similarly argues that visual awareness depends on local feedback loops within the visual areas. Processing in higher areas is related to attention, which is distinct from awareness itself.21 Similarly, Zeki22 has proposed what is called the ‘micro-consciousness’ theory, which suggests that activity in the early visual areas are the correlates of specific conscious percepts.
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Many of these theories are controversial, and some pose conflicts to each other. However, one common theme here is that the neural substrate that supports the processing of visual information itself is sufficient to generate a conscious percept, without the need for further processing in higher cognitive areas. In philosophy, one relevant and perhaps similar theory is representationalism,23,24 which (roughly) holds that the phenomenal character associated with a perceptual event is determined by the content of the relevant representation. Mostly, the relevant representation here refers to the ‘first-order’ representation, i.e., if you are seeing a house, the phenomenal character is determined by the content of the representation that is about the house. There is another kind of representationalism that involves what are called ‘higher-order’ representations, to which we now turn.
Higher-Order Theories According to higher-order representational theories,25–27 in order to have a conscious experience, we need more than just the first-order representation, which has the object of perception as its content. On top of that, we need to have a higher-order representation that is about the first-order representation. There is some debate as to whether the content of this higher-order representation is similar to thoughts25 or percepts,26 or perhaps that the higher-order representation and the first-order representation should not be counted as separate, but rather as parts of a single self-referential system.27 According to the higher-order thought theory, which is arguably the most popular view amongst the different versions, the content of the higher-order representation is something like ‘I think I’m seeing red’, given that the first-order representation is ‘red’. I have put forward a different version of this theory.16 According to this theory, the higher-order representation simply enables statistical inferences or judgments of perceptual certainty. That is, given that the first-order representations are often corrupted by noise in the brain, the higher-order representation contains some statistical information that allows one to say something like ‘this perception (of a house) is likely to be 99% reliable’. Awareness occurs when a percept is correctly judged to be sufficiently reliable. There are, I think, some advantages of this version of higherorder representationalism over the traditional philosophical forms,16 but these are not discussed here. Higher-order theories in general are congenial to the results that a change in activity in the prefrontal and parietal cortices are sufficient for a change in conscious percept (Alternative 2)—one would expect the higher-order representations to be in these brain 4
regions, as they seem to play roles in uncertainty monitoring, cognitive control, thinking and planning, etc. In particular, some higher-order theorists (myself included) are committed to make the prediction that if one keeps the first-order representation constant, a change in the higher-order representations alone would be enough to change the character of a conscious experience.d This last point is important and is perhaps what distinguishes at least some higher-order theories from the global workspace theory. It is unclear whether the global workspace theory is committed to such predictions. In most discussions, one typically thinks that a visual signal (roughly equivalent to a first-order representation) enters the global workspace by being stronger than other competing signals. Therefore, when a visual percept changes from consciously seen to unseen, one would expect the difference to be reflected not only in the higher global workspace areas, but in the lower visual signals too. Also, it may be possible that when the signal enters the workspace, the global broadcasting sends feedback to the earlier visual areas, which would in turn mean that the conscious signal would end up becoming stronger in the early areas. Even when the first-order visual signal is the same, and somehow in one condition the signal gets into the workspace and in another condition it does not, one would predict big behavioral differences, such as that in one condition the visual targets are better identified or reported, because the workspace is supposed to be functionally important. The higher-order theory (at least the version I put forward), however, would expect that there can be few functional differences in terms of discrimination, identification, or ability to report the target, if the first-order signal/representation is kept the same. A difference in higher-order representation leads to a difference in awareness, and the only accompanying behavioral difference is the judgment of perceptual certainty. For example, the subject reports ‘red’ in both cases with equal accuracy across many trials, except that with the right higher-order representation the subject would say ‘I’m consciously seeing red and I’m confident that I’m right’; while with the faulty higher-order representation the subject would say ‘I don’t consciously see anything but if you force me to guess, my hunch is there’s something red’.
DUAL CHANNEL VERSUS HIERARCHICAL PROCESSING The last point is critically relevant to what the difference is between normal vision and blindsight.
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One advantage of higher-order theory is that it explains blindsight behavior most naturally. In blindsight, the performance capacity is above chance, presumably because some residual visual signal (firstorder representations) still exists. What are missing are the relevant higher-order representations (perhaps because the cortical signal is disturbed due to the damage in V1), which leads to a dramatically reduced level of perceptual certainty. In fact, one can have perfectly matched performance capacity between blindsight and normal vision (by for instance presenting a strong stimulus to blindsighted vision and a weak stimulus to normal vision), and the prediction would be that the difference in awareness would be reflected in the prefrontal and parietal areas. Indeed, there is some evidence supporting this.18,28 How would the global workspace theory account for this kind of performance-matched condition where the subjectively reported levels of awareness differ dramatically? If the visual signal (first-order representation) itself is the same, and that gets into the workspace in one condition but not the other, one would expect a difference in performance capacity because the workspace is supposed to contribute to that. One could perhaps maintain that some signal can get into the workspace, and thereby render itself conscious, without influencing task performance. However, the main point of the workspace is to amplify and broadcast the signal, for functional reasons. If one allows signal to enter the workspace without having any functional consequence but just to make itself conscious, it would no longer be in the spirit of the workspace theory. Recently, one of the major proponents of the global workspace theory, Stanislas Dehaene, together with colleagues, has proposed a dual-channel model that would account for unconscious but functionally strong behavior.14 Essentially, the idea is that sometimes the signal can enter some other channel rather than the global workspace, which can also contribute to performance capacity. Allowing for such a ‘backdoor’ of information processing somewhat makes the global workspace not so ‘global’, but this accounts for phenomena such as blindsight. It should be easy to see that this dual-channel structure is a natural solution for the local theorist too. According to them, the early visual signal itself (the first-order representation) is sufficient for visual awareness. So how can one explain blindsight then? How can you have a visual signal without awareness? Presumably, some other visual signal, perhaps carried by a different kind of neural substrate that does not lead to awareness, would do the unconscious job. Vo lu me 2, Jan u ary /Febru ary 2011
This again means that there are different channels of processing, some conscious and some not. Local theorists may try to argue that the same sensory signal is partially impaired in blindsight, which leads to unawareness. For instance, it could be that feedback processing to V1 is no longer possible, which leads to unawareness. However, if feedback to V1 is part of the signal, when this breaks down one would expect performance to go down as well. The focus here is on how to explain performance-matched cases of difference in awareness. In such cases, it would be natural for local theorists to assume that some other ‘unconscious’ signal arises to compensate for the loss of the ‘conscious’ signal. This is the critical point where the higher-order theories differ from both the global and local theories. According to higher-order theories, one could have exactly the same channel, but some late stage of processing up in the hierarchy (the higher-order representation stage) differs, and this is all that is sufficient to render a conscious percept unconscious. In fact, there are some preliminary results from my laboratory, using computational modeling, which suggest that a hierarchical model of processing is more realistic than a dual-channel model in terms of accounting for the differences between conscious and unconscious vision.29 In neural terms, this means that the burden falls on global and local theorists to identify neural substrates in presumably different neuronal populations that subserve unconscious visual behavior, as their theories seem to require a different channel for unconscious processing. The higher-order theorists (or at least some of them) are not committed to this. A subject could have exactly the same visual processing in visual and subcortical areas, and so long as some activity in higher-order monitoring areas differs, one could render normal vision unconscious.
CONCLUDING REMARKS I do not pretend that this is an unbiased review. It should come as no surprise that the author prefers the higher-order theory, and I think that one could keep the visual activity constant and yet manipulate visual phenomenology by changing the activity in prefrontal and parietal areas. On some occasions, to support such opinions I even appeal to preliminary data (i.e., conference posters and abstracts, but not full published papers). But opinions aside, the main point of the article is not to convince you that one theory is right over the others. The point is that by studying the NCC, one could, in fact, make theoretical contributions.
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However, as we look into this issue in more detail, it may become obvious that the problem does not afford such a clean-cut solution. It is not as if the problem of deciding different views of the NCC can be resolved solely by experimental labor. The issue often involves deciding what counts as an experimental confound and what counts as a good experiment. Should we distinguish between attention and awareness, or treat them as the same? Is awareness the same as performance capacity? When we keep the stimulus constant, and compare ‘hits’ versus ‘misses’, are we looking at awareness, or just spontaneous fluctuations of the signal strength? I have given arguments elsewhere30 to support my view that comparing ‘hits’ versus ‘misses’ is perhaps flawed (it studies performance capacity but not awareness per se), and that perceptual certainty is probably what tracks the subjective aspects of awareness best. But these arguments are controversial, and I do not wish to repeat them here. It may be unfortunate that we cannot just quickly and unanimously derive some empirical predictions based on the theories, and arbitrate them by some uncontroversial experiments on the NCC. The search for the NCC is bound to involve conceptual problems. But if anything, I hope I have convinced some readers that the search for the NCC is not completely irrelevant to our theoretical understanding of the nature of perceptual awareness. The future depends much on the interplay between both theory and empirical studies.
NOTES a
The result was independently predicted by philosopher Uriah Kriegel.31
b
For most of the discussion on the relationship between theories and views of NCCs, one could think of the theory as predicting a certain NCC to be the necessary condition for consciousness to arise. In this case of the global workspace theory, though, it is not entirely clear whether all global theorists hold that early visual activity is necessary. That is, such an activity could be the normal cause that leads to global activity in the prefrontal and parietal cortex, which in turn is necessary for consciousness. c Technically, Block’s theory is about the experiential/phenomenological aspect of consciousness whereas the global workspace theory concerns conscious access of information. So in one sense, the two theories do not contradict. However, many who reject Block’s theory also reject his distinction of phenomenology versus access; many would say phenomenology that is not accessible should not be considered conscious at all. Therefore, Block’s theory and the global workspace theory are often seen as in competition. d Theorists like myself and Uriah Kriegel predict this to be the case because we think the overall phenomenology, i.e., content of awareness, is determined jointly by the first-order and higher-order representations. In my view specifically, I think the higher-order representations do not duplicate the perceptual content of the first-order representations. Rather, metaphorically speaking, they add a ‘label’ to the first-order representations to explicitly indicate how reliable they are. Higher-order thought theorist David Rosenthal, on the other hand, holds that the content of the higherorder representation alone is sufficient to determine the content of awareness.
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